Interspecific competition shapes bird species' distributions along tropical precipitation gradients.

The hypothesis that species' ranges are limited by interspecific competition has motivated decades of debate, but a general answer remains elusive. Here we test this hypothesis for lowland tropical birds by examining species' precipitation niche breadths. We focus on precipitation because it-not temperature-is the dominant climate variable that shapes the biota of the lowland tropics. We used 3.6 million fine-scale citizen science records from eBird to measure species' precipitation niche breadths in 19 different regions across the globe. Consistent with the predictions of the interspecific competition hypothesis, multiple lines of evidence show that species have narrower precipitation niches in regions with more species. This means species inhabit more specialized precipitation niches in species-rich regions. We predict this niche specialization should make tropical species in high diversity regions disproportionately vulnerable to changes in precipitation regimes; preliminary empirical evidence is consistent with this prediction.

Avian diversity and function across the world's most populous cities.

Understanding the composition of urban wildlife communities is crucial to promote biodiversity, ecosystem function and links between nature and people. Using crowdsourced data from over five million eBird checklists, we examined the influence of urban characteristics on avian richness and function at 8443 sites within and across 137 global cities. Under half of the species from regional pools were recorded in cities, and we found a significant phylogenetic signal for urban tolerance. Site-level avian richness was positively influenced by the extent of open forest, cultivation and wetlands and avian functional diversity by wetlands. Functional diversity co-declined with richness, but groups including granivores and aquatic birds occurred even at species-poor sites. Cities in arid areas held a higher percentage of regional species richness. Our results indicate commonalities in the influence of habitat on richness and function, as well as lower niche availability, and phylogenetic diversity across the world's cities.

Evolution of Brain-Expressed Biogenic Amine Receptors into Olfactory Trace Amine-Associated Receptors.

The family of trace amine-associated receptors (TAARs) is distantly related to G protein-coupled biogenic aminergic receptors. TAARs are found in the brain as well as in the olfactory epithelium where they detect biogenic amines. However, the functional relationship of receptors from distinct TAAR subfamilies and in different species is still uncertain. Here, we perform a thorough phylogenetic analysis of 702 TAAR-like (TARL) and TAAR sequences from 48 species. We show that a clade of Tarl genes has greatly expanded in lampreys, whereas the other Tarl clade consists of only one or two orthologs in jawed vertebrates and is lost in amniotes. We also identify two small clades of Taar genes in sharks related to the remaining Taar genes in bony vertebrates, which are divided into four major clades. We further identify ligands for 61 orphan TARLs and TAARs from sea lamprey, shark, ray-finned fishes, and mammals, as well as novel ligands for two 5-hydroxytryptamine receptor 4 orthologs, a serotonin receptor subtype closely related to TAARs. Our results reveal a pattern of functional convergence and segregation: TARLs from sea lamprey and bony vertebrate olfactory TAARs underwent independent expansions to function as chemosensory receptors, whereas TARLs from jawed vertebrates retain ancestral response profiles and may have similar functions to TAAR1 in the brain. Overall, our data provide a comprehensive understanding of the evolution and ligand recognition profiles of TAARs and TARLs.

Synergism, Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors.

Sensory receptor evolution can imply trade-offs between ligands, but the extent to which such trade-offs occur and the underlying processes shaping their evolution is not well understood. For example, hummingbirds have repurposed their ancestral savory receptor (T1R1-T1R3) to detect sugars, but the impact of this sensory shift on amino acid perception is unclear. Here, we use functional and behavioral approaches to show that the hummingbird T1R1-T1R3 acts as a bifunctional receptor responsive to both sugars and amino acids. Our comparative analyses reveal substantial functional diversity across the hummingbird radiation and suggest an evolutionary timeline for T1R1-T1R3 retuning. Finally, we identify a novel form of synergism between sugars and amino acids in vertebrate taste receptors. This work uncovers an unexplored axis of sensory diversity, suggesting new ways in which nectar chemistry and pollinator preferences can coevolve.

The effect of sociality on competitive interactions among birds.

Sociality can provide many benefits, including increased foraging success, reproductive opportunities and defence against predation. How does sociality influence the dominance hierarchies of ecological competitors? Here, we address this question using a large citizen science dataset of competitive interactions among birds foraging at backyard feeders, representing a network of over 55 000 interactions among 68 common species. We first show that species differ in average group size (the number of conspecifics observed together) as a fundamental measure of sociality. When analysing heterospecific competition, we find that sociality is inversely related to dominance. On average, a single individual from a solitary species is more likely to displace a size-matched opponent than a single individual from a social species. Yet, we find that social species gain an increase in their competitive advantage when in the presence of their conspecifics, which may occur as a result of dynamics within their groups. Finally, we show that more social species have relatively fewer dominance interactions with heterospecifics, and more with conspecifics. Overall, these results demonstrate that sociality can influence competition in ecological networks. More social species have decreased competitive ability as individuals, but they may gain competitive ability in groups.

Gut microbiome composition better reflects host phylogeny than diet diversity in breeding wood-warblers.

Understanding the factors that shape microbiomes can provide insight into the importance of host-symbiont interactions and on co-evolutionary dynamics. Unlike for mammals, previous studies have found little or no support for an influence of host evolutionary history on avian gut microbiome diversity and instead have suggested a greater influence of the environment or diet due to fast gut turnover. Because effects of different factors may be conflated by captivity and sampling design, examining natural variation using large sample sizes is important. Our goal was to overcome these limitations by sampling wild birds to compare environmental, dietary and evolutionary influences on gut microbiome structure. We performed faecal metabarcoding to characterize both the gut microbiome and diet of 15 wood-warbler species across a 4-year period and from two geographical localities. We find host taxonomy generally explained ~10% of the variation between individuals, which is ~6-fold more variation of any other factor considered, including diet diversity. Further, gut microbiome similarity was more congruent with the host phylogeny than with host diet similarity and we found little association between diet diversity and microbiome diversity. Together, our results suggest evolutionary history is the strongest predictor of gut microbiome differentiation among wood-warblers. Although the phylogenetic signal of the warbler gut microbiome is not very strong, our data suggest that a stronger influence of diet (as measured by diet diversity) does not account for this pattern. The mechanism underlying this phylogenetic signal is not clear, but we argue host traits may filter colonization and maintenance of microbes.

Systems biology as a framework to understand the physiological and endocrine bases of behavior and its evolution-From concepts to a case study in birds.

Organismal behavior, with its tremendous complexity and diversity, is generated by numerous physiological systems acting in coordination. Understanding how these systems evolve to support differences in behavior within and among species is a longstanding goal in biology that has captured the imagination of researchers who work on a multitude of taxa, including humans. Of particular importance are the physiological determinants of behavioral evolution, which are sometimes overlooked because we lack a robust conceptual framework to study mechanisms underlying adaptation and diversification of behavior. Here, we discuss a framework for such an analysis that applies a "systems view" to our understanding of behavioral control. This approach involves linking separate models that consider behavior and physiology as their own networks into a singular vertically integrated behavioral control system. In doing so, hormones commonly stand out as the links, or edges, among nodes within this system. To ground our discussion, we focus on studies of manakins (Pipridae), a family of Neotropical birds. These species have numerous physiological and endocrine specializations that support their elaborate reproductive displays. As a result, manakins provide a useful example to help imagine and visualize the way systems concepts can inform our appreciation of behavioral evolution. In particular, manakins help clarify how connectedness among physiological systems-which is maintained through endocrine signaling-potentiate and/or constrain the evolution of complex behavior to yield behavioral differences across taxa. Ultimately, we hope this review will continue to stimulate thought, discussion, and the emergence of research focused on integrated phenotypes in behavioral ecology and endocrinology.

Seasonal species richness of birds on the world's islands and its geographical correlates.

The presence of migratory birds on islands results in seasonal variation in species richness. These patterns and their geographical correlates within the context of island biogeography theory have not been examined. We used 21 years of bird observations on 690 islands from eBird to determine how seasonal species richness estimates vary as a function of island area, isolation and latitude. Species richness was highest on islands within the northern mid-latitudes during migration and on islands within tropical latitudes during the non-breeding season. Area defined positive, nonlinear relationships with species richness across seasons, with the steepest slopes occurring with islands greater than 1100 km2. Distance to mainland defined negative, nonlinear relationships with species richness across seasons, with the strongest slopes occurring with islands located greater than 150 km from the mainland. Species-area relationships were weakest for the most remote islands and strongest for islands at intermediate distances to the mainland. Intermediate proximity to other islands was a poor predictor of species richness. Our findings emphasize the presence of seasonally dynamic geographical relationships, the enhanced role of evolutionary processes on larger islands, the unique ecology of the world's most remote islands, and the importance of islands as stopover sites and wintering grounds for migratory bird species.

Macroevolutionary diversification rates show time dependency.

For centuries, biologists have been captivated by the vast disparity in species richness between different groups of organisms. Variation in diversity is widely attributed to differences between groups in how fast they speciate or go extinct. Such macroevolutionary rates have been estimated for thousands of groups and have been correlated with an incredible variety of organismal traits. Here we analyze a large collection of phylogenetic trees and fossil time series and describe a hidden generality among these seemingly idiosyncratic results: speciation and extinction rates follow a scaling law in which both depend on the age of the group in which they are measured, with the fastest rates in the youngest clades. Using a series of simulations and sensitivity analyses, we demonstrate that the time dependency is unlikely to be a result of simple statistical artifacts. As such, this time scaling is likely a genuine feature of the tree of life, hinting that the dynamics of biodiversity over deep time may be driven in part by surprisingly simple and general principles.

Artificial night light and anthropogenic noise interact to influence bird abundance over a continental scale.

The extent of artificial night light and anthropogenic noise (i.e., "light" and "noise") impacts is global and has the capacity to threaten species across diverse ecosystems. Existing research involving impacts of light or noise has primarily focused on noise or light alone and single species; however, these stimuli often co-occur and little is known about how co-exposure influences wildlife and if and why species may vary in their responses. Here, we had three aims: (1) to investigate species-specific responses to light, noise, and the interaction between the two using a spatially explicit approach to model changes in abundance of 140 prevalent bird species across North America, (2) to investigate responses to the interaction between light exposure and night length, and (3) to identify functional traits and habitat affiliations that explain variation in species-specific responses to these sensory stimuli with phylogenetically informed models. We found species that responded to noise exposure generally decreased in abundance, and the additional presence of light interacted synergistically with noise to exacerbate its negative effects. Moreover, the interaction revealed negative emergent responses for several species that only reacted when light and noise co-occurred. Additionally, an interaction between light and night length revealed 47 species increased in abundance with light exposure during longer nights. In addition to modifying behavior with optimal temperature and potential foraging opportunities, birds might be attracted to light, yet suffer inadvertent physiological consequences. The trait that most strongly related to avian response to light and noise was habitat affiliation. Specifically, species that occupy closed habitat were less tolerant of both sensory stressors compared to those that occupy open habitat. Further quantifying the contexts and intrinsic traits that explain how species respond to noise and light will be fundamental to understanding the ecological consequences of a world that is ever louder and brighter.

Does variation in glucocorticoid concentrations predict fitness? A phylogenetic meta-analysis.

Glucocorticoid hormones (GCs) are central mediators of metabolism and the response to challenges. Because circulating GC levels increase in response to challenges, within-population variation in GCs could reflect among-individual variation in condition or experience. At the same time, individual variation in GC regulation could have causal effects on energetic balance or stress coping capacity in ways that influence fitness. Although a number of studies in vertebrates have tested whether variation in GCs among individuals predicts components of fitness, it is not clear whether there are consistent patterns across taxa. Here we present the first phylogenetic meta-analysis testing whether variation in GCs is associated with survival and reproductive success across vertebrates. At the same time, we introduce and test predictions about a potentially important mediator of GC-fitness relationships: life history context. We suggest that strong context-dependence in the fitness benefit of maintaining elevated GCs could obscure consistent patterns between GCs and fitness across taxa. Meta-analyses revealed that baseline and stress-induced GCs were consistently negatively correlated with reproductive success. This relationship did not differ depending on life history context. In contrast, the relationships between GCs and survival were highly context dependent, differing according to life history strategy. Both baseline and stress-induced GCs were more strongly negatively associated with survival in longer-lived populations and species. Stress-induced GCs were also more positively associated with survival in organisms that engage in relatively more valuable reproductive attempts. Fecal GCs did not correlate with survival or reproductive success. We also found that experimental increases in GCs reduced both survival and reproductive success; however, evidence of publication bias and the small sample size suggest that more data is required to confirm this conclusion. Overall, these results support the prediction that GC-fitness relationships can be strongly context dependent, and suggest that incorporating life history may be particularly important for understanding GC-survival relationships.

Macroevolutionary Patterning in Glucocorticoids Suggests Different Selective Pressures Shape Baseline and Stress-Induced Levels.

Glucocorticoid (GC) hormones are important phenotypic mediators across vertebrates, but their circulating concentrations can vary markedly. Here we investigate macroevolutionary patterning in GC levels across tetrapods by testing seven specific hypotheses about GC variation and evaluating whether the supported hypotheses reveal consistent patterns in GC evolution. If selection generally favors the "supportive" role of GCs in responding effectively to challenges, then baseline and/or stress-induced GCs may be higher in challenging contexts. Alternatively, if selection generally favors "protection" from GC-induced costs, GCs may be lower in environments where challenges are more common or severe. The predictors of baseline GCs were all consistent with supportive effects: levels were higher in smaller organisms and in those inhabiting more energetically demanding environments. During breeding, baseline GCs were also higher in populations and species with fewer lifetime opportunities to reproduce. The predictors of stress-induced GCs were instead more consistent with the protection hypothesis: during breeding, levels were lower in organisms with fewer lifetime reproductive opportunities. Overall, these patterns indicate a surprising degree of consistency in how some selective pressures shape GCs across broad taxonomic scales; at the same time, in challenging environments selection appears to operate on baseline and stress-induced GCs in distinct ways.

Evolution of a multifunctional trait: shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution.

While morphological traits are often associated with multiple functions, it remains unclear how evolution balances the selective effects of different functions. Birds' beaks function not only in foraging but also in thermoregulating and singing, among other behaviours. Studies of beak evolution abound, however, most focus on a single function. Hence, we quantified relative contributions of different functions over an evolutionary timescale. We measured beak shape using geometric morphometrics and compared this trait with foraging behaviour, climatic variables and song characteristics in a phylogenetic comparative study of an Australasian radiation of songbirds (Meliphagidae). We found that both climate and foraging behaviour were significantly correlated with the beak shape and size. However, foraging ecology had a greater effect on shape, and climate had a nearly equal effect on size. We also found that evolutionary changes in beak morphology had significant consequences for vocal performance: species with elongate-shaped beaks sang at higher frequencies, while species with large beaks sang at a slower pace. The evolution of the avian beak exemplifies how morphological traits can be an evolutionary compromise among functions, and suggests that specialization along any functional axis may increase ecological divergence or reproductive isolation along others.

The Evolution of Energetic Scaling across the Vertebrate Tree of Life.

Metabolism is the link between ecology and physiology-it dictates the flow of energy through individuals and across trophic levels. Much of the predictive power of metabolic theories of ecology derives from the scaling relationship between organismal size and metabolic rate. There is growing evidence that this scaling relationship is not universal, but we have little knowledge of how it has evolved over macroevolutionary time. Here we develop a novel phylogenetic comparative method to investigate how often and in which clades the macroevolutionary dynamics of the metabolic scaling have changed. We find strong evidence that the metabolic scaling relationship has shifted multiple times across the vertebrate phylogeny. However, shifts are rare and otherwise strongly constrained. Importantly, both the estimated slope and intercept values vary widely across regimes, with slopes that spanned across theoretically predicted values such as 2/3 or 3/4. We further tested whether traits such as ecto-/endothermy, genome size, and quadratic curvature with body mass (i.e., energetic constraints at extreme body sizes) could explain the observed pattern of shifts. Though these factors help explain some of the variation in scaling parameters, much of the remaining variation remains elusive. Our results lay the groundwork for further exploration of the evolutionary and ecological drivers of major transitions in metabolic strategy and for harnessing this information to improve macroecological predictions.

Radiating despite a Lack of Character: Ecological Divergence among Closely Related, Morphologically Similar Honeyeaters (Aves: Meliphagidae) Co-occurring in Arid Australian Environments.

Quantifying the relationship between form and function can inform use of morphology as a surrogate for ecology. How the strength of this relationship varies continentally can inform understanding of evolutionary radiations; for example, does the relationship break down when certain lineages invade and diversify in novel habitats? The 75 species of Australian honeyeaters (Meliphagidae) are morphologically and ecologically diverse, with species feeding on nectar, insects, fruit, and other resources. We investigated Meliphagidae ecomorphology and community structure by (1) quantifying the concordance between morphology and ecology (foraging behavior), (2) estimating rates of trait evolution in relation to the packing of ecological space, and (3) comparing phylogenetic and trait community structure across the broad environmental gradients of the continent. We found that morphology explained 37% of the variance in ecology (and 62% vice versa), and we uncovered well-known bivariate relationships among the multivariate ecomorphological data. Ecological trait diversity declined less rapidly than phylogenetic diversity along a gradient of decreasing precipitation. We employ a new method (trait fields) and extend another (phylogenetic fields) to show that while species in phylogenetically clustered, arid-environment assemblages are similar morphologically, they are as varied in foraging behavior as those from more diverse assemblages. Thus, although closely related and similar morphologically, these arid-adapted species have diverged in ecological space to a similar degree as their mesic counterparts.

Paraphyly changes understanding of timing and tempo of diversification in subtribe Hakeinae (Proteaceae), a giant Australian plant radiation.

PREMISE OF THE STUDY: Subtribe Hakeinae (526 spp.) represents a large Australian plant radiation central to our understanding of that flora's evolution and ecology. It contains Grevillea-the third largest plant genus in Australia and a group inferred to have among the highest diversification rates in the angiosperms. However, we lack a robust phylogenetic framework for understanding subtribe Hakeinae and recognize that Grevillea lacks an unambiguous synapomorphy supporting its monophyly. METHODS: We used four plastid and one nuclear DNA region from a taxonomically even sampling of a third of the species to infer a time-calibrated phylogeny of Hakeinae and absolute diversification rates of major clades. We developed the R package addTaxa to add unsampled taxa to the tree for diversification rate inference. KEY RESULTS: Grevillea is paraphyletic with respect to Hakea and Finschia. Under most parameter combinations, Hakea contains the major clade with the highest diversification rate in Hakeinae, rather than Grevillea. The crown age of the Grevillea+Hakea+Finschia crown group is about double that of prior estimates. CONCLUSIONS: We demonstrate that the paraphyly of Grevillea considerably enlarges the number of Australian descendants from its most recent common ancestor but has also misled investigators who considered a single operational taxonomic unit as adequate to represent the genus for inferences of diversification rate and timing. Our time-calibrated phylogeny can form the basis of future evolutionary, comparative ecology, and biogeography studies involving this large Australian plant radiation, as well as nomenclatural changes.

Unfamiliarity generates costly aggression in interspecific avian dominance hierarchies.

Dominance hierarchies often form between species, especially at common feeding locations. Yet, relative to work focused on the factors that maintain stable dominance hierarchies within species, large-scale analyses of interspecific dominance hierarchies have been comparatively rare. Given that interspecific behavioral interference mediates access to resources, these dominance hierarchies likely play an important and understudied role in community assembly and behavioral evolution. To test alternative hypotheses about the formation and maintenance of interspecific dominance hierarchies, we employ an large, participatory science generated dataset of displacements observed at feeders in North America in the non-breeding season. Consistent with the hypothesis that agonistic interference can be an adaptive response to exploitative competition, we find that species with similar niches are more likely to engage in costly aggression over resources. Among interacting species, we find broad support for the hypothesis that familiarity (measured as fine-scale habitat overlap) predicts adherence to the structure of the dominance hierarchy and reduces aggression between species. Our findings suggest that the previously documented agonistic hierarchy in North American birds emerges from species-level adaptations and learned behaviors that result in the avoidance of costly aggression.